Electrical fields in wound healing—An overriding signal that directs cell migration

Eaglstein, 1997, Chronic wounds, Surg Clin North Am, 77, 689, 10.1016/S0039-6109(05)70575-2 Falanga, 1993, The “trap” hypothesis of venous ulceration, Lancet, 341, 1006, 10.1016/0140-6736(93)91085-Z Singer, 1999, Cutaneous wound healing, N Engl J Med, 341, 738, 10.1056/NEJM199909023411006 Macaluso DC, Feldman ST. Pathogenesis of sterile corneal erosions and ulcerations. In: Krachmer JH, Mannis MJ, Holland EJ, editors. Cornea: Fundamentals of cornea and external disease. St. Louis: Mosby-Year Book; 1997. p. 199–212. Ramamurthi, 2006, Pathogenesis, clinical features and management of recurrent corneal erosions, Eye, 20, 635, 10.1038/sj.eye.6702005 Singer, 2002, Determinants of poor outcome after laceration and surgical incision repair, Plast Reconstr Surg, 110, 427, 10.1097/00006534-200208000-00008 Hanna, 1966, Proliferation and migration of epithelial cells during corneal wound repair in the rabbit and the rat, Am J Ophthalmol, 61, 55, 10.1016/0002-9394(66)90747-1 Seiler, 1989, Impaired migration of epidermal cells from decubitus ulcers in cell cultures: a cause of protracted wound healing?, Am J Clin Pathol, 92, 430, 10.1093/ajcp/92.4.430 Woodley, 1996 Fenteany, 2000, Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets, Curr Biol, 10, 831, 10.1016/S0960-9822(00)00579-0 Martin, 1997, Wound healing–aiming for perfect skin regeneration, Science (New York, NY), 276, 75, 10.1126/science.276.5309.75 Gurtner, 2008, Wound repair and regeneration, Nature, 453, 314, 10.1038/nature07039 Jaffe, 1977, Electrical controls of development, Ann Rev Biophys Bioeng, 6, 445, 10.1146/annurev.bb.06.060177.002305 Borgens, 1979, Role of subdermal current shunts in the failure of frogs to regenerate, J Exp Zool, 209, 49, 10.1002/jez.1402090106 Jaffe, 1981, Control of development by steady ionic currents, Fed Proc, 40, 125 Jaffe, 1984, Electric fields and wound healing, Clin Dermatol, 2, 34, 10.1016/0738-081X(84)90025-7 Nishimura, 1996, Human keratinocytes migrate to the negative pole in direct current electric fields comparable to those measured in mammalian wounds, J Cell Sci, 109, 199, 10.1242/jcs.109.1.199 Fang, 1998, Migration of human keratinocytes in electric fields requires growth factors and extracellular calcium, J Investigat Dermatol, 111, 751, 10.1046/j.1523-1747.1998.00366.x Nuccitelli, 2003, A role for endogenous electric fields in wound healing, Curr Top Dev Biol, 58, 1, 10.1016/S0070-2153(03)58001-2 McCaig, 2002, Has electrical growth cone guidance found its potential?, Trends Neurosci, 25, 354, 10.1016/S0166-2236(02)02174-4 McCaig, 2005, Controlling cell behavior electrically: current views and future potential, Physiol Rev, 85, 943, 10.1152/physrev.00020.2004 Ojingwa, 2003, Electrical stimulation of wound healing, J Invest Dermatol, 121, 1, 10.1046/j.1523-1747.2003.12454.x Zhao, 2006, Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN, Nature, 442, 457, 10.1038/nature04925 Pullar, 2005, Cyclic AMP mediates keratinocyte directional migration in an electric field, J Cell Sci, 118, 2023, 10.1242/jcs.02330 Pullar, 2006, beta4 integrin and epidermal growth factor coordinately regulate electric field-mediated directional migration via Rac1, Mol Biol Cell, 17, 4925, 10.1091/mbc.E06-05-0433 Adams, 2007, H+ pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce Xenopus tail regeneration, Development, 134, 1323, 10.1242/dev.02812 Levin, 2007, Large-scale biophysics: ion flows and regeneration, Trends Cell Biol, 17, 261, 10.1016/j.tcb.2007.04.007 Zhao, 1999, Electric field-directed cell motility involves up-regulated expression and asymmetric redistribution of the epidermal growth factor receptors and is enhanced by fibronectin and laminin, Mol Biol Cell, 10, 1259, 10.1091/mbc.10.4.1259 Pu, 2007, EGF receptor signalling is essential for electric-field-directed migration of breast cancer cells, J Cell Sci, 120, 3395, 10.1242/jcs.002774 Scott Stewart, 2007, Bioelectricity and epimorphic regeneration, BioEssays, 29, 1133, 10.1002/bies.20656 Kloth, 2005, Electrical stimulation for wound healing: a review of evidence from in vitro studies, animal experiments, and clinical trials, Int J Low Extrem Wounds, 4, 23, 10.1177/1534734605275733 Nuccitelli, 2003, A role for endogenous electric fields in wound healing, Curr Top Dev Biol, 58, 1, 10.1016/S0070-2153(03)58001-2 Du Bois-Reymond, 1843, Vorläufiger Abriss einer Untersuchung uber den sogenannten Froschstrom und die electomotorischen Fische, Ann Phys Chem, 58, 1, 10.1002/andp.18431340102 Du Bois-Reymond E. Untersuchungen uber thierische Elektricitat, Zweiter Band, Zweite Abtheilung (Erste Lieferung). Berlin: Georg Reimer; 1860. Borgens, 1977, Bioelectricity and regeneration: large currents leave the stumps of regenerating newt limbs, Proc Natl Acad Sci USA, 74, 4528, 10.1073/pnas.74.10.4528 Borgens, 1980, Large and persistent electrical currents enter the transected lamprey spinal cord, Proc Natl Acad Sci USA, 77, 1209, 10.1073/pnas.77.2.1209 Borgens, 1983, A steady efflux of ionic current predicts hind limb development in the axolotl, J Exp Zool, 228, 491, 10.1002/jez.1402280309 Borgens, 1984, Endogenous ionic currents traverse intact and damaged bone, Science, 225, 478, 10.1126/science.6740320 Altizer, 2001, Endogenous electric current is associated with normal development of the vertebrate limb, Dev Dyn, 221, 391, 10.1002/dvdy.1158 Jaffe, 1974, An ultrasensitive vibrating probe for measuring steady extracellular currents, J Cell Biol, 63, 614, 10.1083/jcb.63.2.614 Reid, 2007, Non-invasive measurement of bioelectric currents with a vibrating probe, Nat Protoc, 2, 661, 10.1038/nprot.2007.91 Foulds, 1983, Human skin battery potentials and their possible role in wound healing, Br J Dermatol, 109, 515, 10.1111/j.1365-2133.1983.tb07673.x Barker, 1982, The glabrous epidermis of cavies contains a powerful battery, Am J Physiol, 242, R358 Illingworth, 1980, Measurement of electrical currents emerging during the regeneration of amputated finger tips in children, Clin Phys Physiol Measure, 1, 87, 10.1088/0143-0815/1/1/007 Chiang, 1992, Electrical fields in the vicinity of epithelial wounds in the isolated bovine eye, Exp Eye Res, 54, 999, 10.1016/0014-4835(92)90164-N Mukerjee, 2006, Microneedle array for measuring wound generated electric fields, Conf Proc IEEE Eng Med Biol Soc, 1, 4326, 10.1109/IEMBS.2006.260205 Nuccitelli, 2008, Imaging the electric field associated with mouse and human skin wounds, Wound Repair Regen, 16, 432, 10.1111/j.1524-475X.2008.00389.x Levin, 2005, CFTR-regulated chloride transport at the ocular surface in living mice measured by potential differences, Invest Ophthalmol Vis Sci, 46, 1428, 10.1167/iovs.04-1314 Levin, 2006, Potential difference measurements of ocular surface Na+ absorption analyzed using an electrokinetic model, Invest Ophthalmol Vis Sci, 47, 306, 10.1167/iovs.05-1082 Candia, 2004, Electrolyte and fluid transport across corneal, conjunctival and lens epithelia, Exp Eye Res, 78, 527, 10.1016/j.exer.2003.08.015 Reinach PS, Capó-Aponte JE, Mergler S, Pokorny KS. Roles of corneal epithelial ion transport mechanisms in mediating responses to cytokines and osmotic stress. In: Ocular transporters in ophthalmic diseases and drug delivery; 2008. p. 17–46. Klyce, 1985, Transport processes across the rabbit corneal epithelium: a review, Curr Eye Res, 4, 323, 10.3109/02713688509025145 Friedman, 1995, Cellular calcium transport in renal epithelia: measurement, mechanisms, and regulation, Physiol Rev, 75, 429, 10.1152/physrev.1995.75.3.429 Garty, 1997, Epithelial sodium channels: function, structure, and regulation, Physiol Rev, 77, 359, 10.1152/physrev.1997.77.2.359 Hoenderop, 2005, Calcium absorption across epithelia, Physiol Rev, 85, 373, 10.1152/physrev.00003.2004 Kunzelmann, 2002, Electrolyte transport in the mammalian colon: mechanisms and implications for disease, Physiol Rev, 82, 245, 10.1152/physrev.00026.2001 Larsen, 1991, Chloride transport by high-resistance heterocellular epithelia, Physiol Rev, 71, 235, 10.1152/physrev.1991.71.1.235 Macknight, 1980, Sodium transport across toad urinary bladder: a model “tight” epithelium, Physiol Rev, 60, 615, 10.1152/physrev.1980.60.3.615 Mathias, 1997, Physiological properties of the normal lens, Physiol Rev, 77, 21, 10.1152/physrev.1997.77.1.21 Reuss, 1989, Ion transport across gallbladder epithelium, Physiol Rev, 69, 503, 10.1152/physrev.1989.69.2.503 Turnheim, 1991, Intrinsic regulation of apical sodium entry in epithelia, Physiol Rev, 71, 429, 10.1152/physrev.1991.71.2.429 Van Driessche, 1985, Ionic channels in epithelial cell membranes, Physiol Rev, 65, 833, 10.1152/physrev.1985.65.4.833 Welsh, 1987, Electrolyte transport by airway epithelia, Physiol Rev, 67, 1143, 10.1152/physrev.1987.67.4.1143 Uyekubo, 1998, cAMP-dependent absorption of chloride across airway epithelium, Am J Physiol, 275, L1219 Maminishkis, 2006, Confluent monolayers of cultured human fetal retinal pigment epithelium exhibit morphology and physiology of native tissue, Invest Ophthalmol Vis Sci, 47, 3612, 10.1167/iovs.05-1622 Hammerton, 1991, Mechanism for regulating cell surface distribution of Na+, K(+)-ATPase in polarized epithelial cells, Science (New York, NY), 254, 847, 10.1126/science.1658934 Shi, 1995, Three-dimensional gradients of voltage during development of the nervous system as invisible coordinates for the establishment of embryonic pattern, Dev Dyn, 202, 101, 10.1002/aja.1002020202 Jaffe, 1979, Strong electrical currents leave the primitive streak of chick embryos, Science (New York, NY), 206, 569, 10.1126/science.573921 Hotary, 1990, Endogenous electrical currents and the resultant voltage gradients in the chick embryo, Dev Biol, 140, 149, 10.1016/0012-1606(90)90062-N Nuccitelli, 1992, Endogenous ionic currents and DC electric fields in multicellular animal tissues, Bioelectromagnetics, Supp. 1, 147, 10.1002/bem.2250130714 Vanable, 1989 Candia, 1968, Electrical potential profile of the isolated frog cornea, Invest Ophthalmol, 7, 405 Lindemann, 1968, Resting potential of isolated beef cornea, Exp Eye Res, 7, 62, 10.1016/S0014-4835(68)80027-2 Chiang, 1991, Intrinsic electric fields promote epithelization of wounds in the newt Notophthalmus viridescens, Dev Biol, 146, 377, 10.1016/0012-1606(91)90239-Y Reid, 2005, Wound healing in rat cornea: the role of electric currents, FASEB J, 19, 379, 10.1096/fj.04-2325com Midelfart, 1987, The effect of amiloride on Na, K and water in bovine corneal epithelium, Exp Eye Res, 45, 751, 10.1016/S0014-4835(87)80092-1 Mirshahi, 1999, Immunochemical analysis of the sodium channel in rodent and human eye, Exp Eye Res, 69, 21, 10.1006/exer.1999.0675 Levin, 2006, Aquaporins and CFTR in ocular epithelial fluid transport, J Membr Biol, 210, 105, 10.1007/s00232-005-0849-1 Dunn, 2001, Immunolocalization of the Na–K–Cl cotransporter in bovine ciliary epithelium, Invest Ophthalmol Vis Sci, 42, 343 Zadunaisky, 1966, Active transport of chloride across the cornea, Nature, 209, 1136, 10.1038/2091136b0 Hibino, 2006, Ion flow regulates left–right asymmetry in sea urchin development, Dev Genes Evol, 216, 265, 10.1007/s00427-005-0051-6 Schaeffer, 1986, Mechanism for leukotriene C4 stimulation of chloride transport in cornea, J Membr Biol, 93, 229, 10.1007/BF01871177 Klyce, 1973, The activation of chloride transport by epinephrine and Db cyclic-AMP in the cornea of the rabbit, Invest Ophthalmol, 12, 127 Talluri, 2006, Mechanism of L-ascorbic acid uptake by rabbit corneal epithelial cells: evidence for the involvement of sodium-dependent vitamin C transporter 2, Curr Eye Res, 31, 481, 10.1080/02713680600693629 Scott, 1975, Ascorbic acid stimulates chloride transport in the amphibian cornea, Invest Ophthalmol, 14, 763 Klyce, 1982, Effects of Ag+ on ion transport by the corneal epithelium of the rabbit, J Membr Biol, 66, 133, 10.1007/BF01868489 McGahan, 1982, Stimulation of transepithelial sodium and chloride transport by ascorbic acid Induction of Na+ channels is inhibited by amiloride, Biochim Biophys Acta, 689, 385, 10.1016/0005-2736(82)90273-5 Song, 2002, Electrical cues regulate the orientation and frequency of cell division and the rate of wound healing in vivo, Proc Natl Acad Sci USA, 99, 13577, 10.1073/pnas.202235299 Song, 2004, Nerve regeneration and wound healing are stimulated and directed by an endogenous electrical field in vivo, J Cell Sci, 117, 4681, 10.1242/jcs.01341 Epstein, 1985, Na–K–Cl cotransport in chloride-transporting epithelia, Ann N Y Acad Sci, 456, 187, 10.1111/j.1749-6632.1985.tb14864.x Robinson, 1985, The responses of cells to electrical fields: a review, J Cell Biol, 101, 2023, 10.1083/jcb.101.6.2023 Nuccitelli, 1983, Embryonic cell motility can be guided by physiological electric fields, Exp Cell Res, 147, 195, 10.1016/0014-4827(83)90284-7 Gruler, 1991, Neural crest cell galvanotaxis: new data and a novel approach to the analysis of both galvanotaxis and chemotaxis, Cell Motil Cytoskeleton, 19, 121, 10.1002/cm.970190207 Etienne-Manneville, 2001, Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKC, Cell, 106, 489, 10.1016/S0092-8674(01)00471-8 Etienne-Manneville, 2003, Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity, Nature, 421, 753, 10.1038/nature01423 Kupfer, 1982, Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound, Proc Natl Acad Sci USA, 79, 2603, 10.1073/pnas.79.8.2603 Kupfer, 1983, Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets, Proc Natl Acad Sci USA, 80, 7224, 10.1073/pnas.80.23.7224 Nobes, 1999, Rho GTPases control polarity, protrusion, and adhesion during cell movement, J Cell Biol, 144, 1235, 10.1083/jcb.144.6.1235 Ridley, 2003, Cell migration: integrating signals from front to back, Science, 302, 1704, 10.1126/science.1092053 Mellor, 2004, Cell motility: Golgi signalling shapes up to ship out, Curr Biol, 14, R434, 10.1016/j.cub.2004.05.038 Preisinger, 2004, YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3zeta, J Cell Biol, 164, 1009, 10.1083/jcb.200310061 Small, 2002, How do microtubules guide migrating cells?, Nat Rev, 3, 957, 10.1038/nrm971 Small, 2003, Microtubules meet substrate adhesions to arrange cell polarity, Curr Opin Cell Biol, 15, 40, 10.1016/S0955-0674(02)00008-X Efimov, 2007, Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi Network, Dev Cell, 12, 917, 10.1016/j.devcel.2007.04.002 Pu, 2005, Golgi polarization in a strong electric field, J Cell Sci, 118, 1117, 10.1242/jcs.01646 Zhao, 2003, Direct visualization of a stratified epithelium reveals that wounds heal by unified sliding of cell sheets, FASEB J, 17, 397, 10.1096/fj.02-0610com Zhao, 1999, A small, physiological electric field orients cell division, Proc Natl Acad Sci USA, 96, 4942, 10.1073/pnas.96.9.4942 Bai, 2004, DC electric fields induce distinct preangiogenic responses in microvascular and macrovascular cells, Arterioscler Thromb Vasc Biol, 24, 1234, 10.1161/01.ATV.0000131265.76828.8a Zhao, 2004, Electrical stimulation directly induces pre-angiogenic responses in vascular endothelial cells by signaling through VEGF receptors, J Cell Sci, 117, 397, 10.1242/jcs.00868 Zhao, 2006, Electric stimulation and angiogenesis: electrical signals have direct effects on endothelial cells, 495 Song, 2007, Application of direct current electric fields to cells and tissues in vitro and modulation of wound electric field in vivo, Nat Protoc, 2, 1479, 10.1038/nprot.2007.205 Van Haastert, 2004, Chemotaxis: signalling the way forward, Nat Rev, 5, 626, 10.1038/nrm1435 Iglesias, 2008, Navigating through models of chemotaxis, Curr Opi Cell Biol, 20, 35, 10.1016/j.ceb.2007.11.011 Janetopoulos, 2008, Directional sensing during chemotaxis, FEBS Lett, 582, 2075, 10.1016/j.febslet.2008.04.035 Fang, 1999, Epidermal growth factor receptor relocalization and kinase activity are necessary for directional migration of keratinocytes in DC electric fields, J Cell Sci, 112, 1967, 10.1242/jcs.112.12.1967 Zhao, 2002, Membrane lipids, EGF receptors, and intracellular signals colocalize and are polarized in epithelial cells moving directionally in a physiological electric field, FASEB J, 16, 857, 10.1096/fj.01-0811fje Huttenlocher, 2007, Wound healing with electric potential, N Engl J Med, 356, 303, 10.1056/NEJMcibr066496 Brown, 1994, Electric field-directed fibroblast locomotion involves cell surface molecular reorganization and is calcium independent, J Cell Biol, 127, 117, 10.1083/jcb.127.1.117 Pullar, 2001, Cyclic AMP-dependent protein kinase A plays a role in the directed migration of human keratinocytes in a DC electric field, Cell Motil Cytoskel, 50, 207, 10.1002/cm.10009 Nuccitelli, 1993, Protein kinases are required for embryonic neural crest cell galvanotaxis, Cell Motil Cytoskel, 24, 54, 10.1002/cm.970240107 Finkelstein, 2004, Roles of microtubules, cell polarity and adhesion in electric-field-mediated motility of 3T3 fibroblasts, J Cell Sci, 117, 1533, 10.1242/jcs.00986 Fang, 1998, Migration of human keratinocytes in electric fields requires growth factors and extracellular calcium, J Invest Dermatol, 111, 751, 10.1046/j.1523-1747.1998.00366.x Trollinger, 2002, Calcium channel blockers inhibit galvanotaxis in human keratinocytes, J Cell Physiol, 193, 1, 10.1002/jcp.10144 Cooper, 1986, Transmembrane Ca2+ fluxes in the forward and reversed galvanotaxis of fish epidermal cells, Prog Clin Biol Res, 210, 311 Franke, 1990, Galvanotaxis of human granulocytes: electric field jump studies, Eur Biophys J, 18, 335, 10.1007/BF00196924 Mycielska, 2004, Cellular mechanisms of direct-current electric field effects: galvanotaxis and metastatic disease, J Cell Sci, 117, 1631, 10.1242/jcs.01125 Aonuma, 2007, Inhibition of anodic galvanotaxis of green paramecia by T-type calcium channel inhibitors, Z Naturforsch, 62, 93, 10.1515/znc-2007-1-217 Lin, 2008, Lymphocyte electrotaxis in vitro and in vivo, J Immunol, 181, 2465, 10.4049/jimmunol.181.4.2465 Bourne HR. G-proteins and GPCrs: from the beginning. In: Ernst Schering Foundation symposium proceedings; 2006. p. 1–21. Wu, 1995, The G protein beta subunit is essential for multiple responses to chemoattractants in Dictyostelium, J Cell Biol, 129, 1667, 10.1083/jcb.129.6.1667 Zhao, 2002, Genetic analysis of the role of G protein-coupled receptor signaling in electrotaxis, J Cell Biol, 157, 921, 10.1083/jcb.200112070 Erickson, 1984, Embryonic fibroblast motility and orientation can be influenced by physiological electric fields, J Cell Biol, 98, 296, 10.1083/jcb.98.1.296